Lamarck believed that traits acquired during an organism’s lifetime could be passed onto the next generation. Although this idea of the inheritance of acquired characters was discarded due to lack of experimental evidence, Conrad H. Waddington realized its significance. In 1953, he showed that Drosophila melanogaster (wild-type) flies that were heat-shocked produced a Crossveinless (cve; disrupted posterior crossveins) trait. Through repeated selection of this trait with heat-shock, he not only increased its frequency in the population, but also found individuals, from the untreated stock, showed the phenotype. It is this apparent inheritance of an acquired character that is so important to evolutionary theory. Despite the long history of this experiment, little is known about the underlying molecular mechanism for Genetic Assimilation. The main aim of this work was to examine Genetic Assimilation at the molecular level. Revisiting the experiment indicated that the there is much that remains unclear. We have shown that (a) production of cve is strain specific, with the white-eyed lines being vulnerable and the wild-type not. Microarray analysis used to compare RNA expression in the wing discs from both the strains appeared to validate the strain specific nature of the trait. (b) Though the frequency of the cve allele increased in every generation, there was a price that crossveinless flies had to pay, in the form of reduced fitness. (c) Assimilation of cve was found to be heritable but, unlike Waddington’s classic work, it did not tend towards fixation; appearing more like a transient, low penetrance effect. Based on the results from whole-genome re-sequencing on Assimilated cve flies, we propose a model for the production of crossveinless. Single nucleotide variants unique to the assimilated line were found to be spread across three major chromosomes, X, 2 and 3. Cve appears to be a result of widespread heterochromatization of the genome that leads to position effects, which then alter the function of key epigenetic and developmental processes. The results, therefore, not only indicate a polygenic basis for crossveinless but also imply that this stress induced trait affects the fly on a broader scale than it was understood before.